Does
sexual selection cause speciation? This long-standing but controversial
question is receiving a lot of attention currently, partly because of the
special role that mate choice can play in determining gene flow. Sexual
selection is thought to cause reproductive isolation when male mating signals
and female preferences diversify because that can lead to sexual isolation
among populations. After many years of relative obscurity this question is now
in the limelight, and evidence is beginning to accumulate in its support. Yet
for the most part, this evidence is limited to inferring a role for sexual
selection when mating traits differ between closely related species that avoid
mating with each other. We remain remarkably ignorant of how sexual selection
causes reproductive isolation and when it is likely to do so. We lack answers
to fundamental questions such as: Is sexual selection a primary driver of
speciation, or is it limited to certain taxa or circumstances? How important is
it relative to natural selection or drift? If sexual selection is involved, is
it arbitrary with respect to environment or is ultimately the product of
ecologically-based divergent selection? Which kinds of sexual selection play a
role -- sexual selection by sensory drive, good genes, or sexual conflict? What
is the genetic basis of traits that confer sexual isolation?

Work in
my lab tackles these questions directly. We investigate behavioral and
ecological causes of divergence in mating traits, the genetic basis of traits
involved in sexual isolation, and are using a comparative approach to evaluate
the generality of early results from model systems. To address these questions
we use a combination of field observations and experiments, laboratory
experiments, quantitative and molecular genetics, and comparative methods. We
work at the intersection of several fields, incorporating conceptual
underpinnings and methodology from evolutionary genetics, evolutionary ecology,
behavioral ecology, and sensory biology. This highly integrative and multilevel
approach has proven powerful for uncovering the processes guiding the evolution
of behavior and the processes of speciation.

My lab
uses an ideal system to study these questions -- species pairs of stickleback
fish (Gasterosteus spp.) found in the
postglacial lakes of British Columbia. These are extremely young species --
less than 13,000 years old -- providing a window on the speciation process.
Evolutionary replication (7 species pairs of sympatric limnetic and benthic
sticklebacks) allows direct experiments to test the evolutionary mechanisms
involved. We also capitalize on genomic tools available for the threespine
stickleback, which has been developed into a premier system for studying the genetics
of adaptation.

Male competition’s effect on
speciation has been almost completely overlooked, despite its direct effect on male reproductive success and despite the prominent
role other forms of competition play in speciation. Our lab has conducted several studies that we hope will change this. We have
evidence that different habitats alter male competition in a manner that generates divergent selection. We have also explored the
fitness landscapes generated by male competition, and find rugged landscapes with multiple fitness peaks, again creating strong
disruptive selection on multiple phenotypic traits.

Genetics and genomics of speciation

This work is designed to understand the genetics of species differences in traits that confer sexual
isolation in sticklebacks. The very recent origin of the stickleback species allows us to investigate
the genetic changes that occur during the process of speciation, especially exciting as a counterpoint
to work on the genetics of speciation in model taxa (e.g., Drosophila) where species are millions of
years old and there is extensive intrinsic genetic isolation. Moreover, much work on the genetics of
speciation ignores the evolutionary causes of genetic change. Our work starts by identifying those causes
and their effect on phenotypes, and then explores the way this shapes the genome. We are characterizing
the genetic architecture of traits known to isolate the species, such as male nuptial color, body size,
and shape, as well as behavioral traits. We use a combination of quantitative genetics, QTL mapping, and
admixture mapping to achieve these goals. This work is relevant to testing several models of speciation,
and will lay the foundation for further work investigating sexual selection and speciation. Our eventual
aim is twofold: to find the genomic regions responsible for mating trait differences, and explore how
selection has acted on those regions to structure the genome.

We have used admixture mapping to uncover the genetic architecture of divergent adaptation and
reproductive isolation. This innovative approach takes advantage of hybridization that occurs between
species in the wild to find genomic regions that underpin species differences. Historically, the
benthic–limnetic species pair from Enos Lake showed strong divergence in many phenotypes, including
male nuptial coloration and body shape, two traits known to be important in speciation. However,
recent ecological disturbance caused extensive hybridization resulting in a single, admixed population.
Using admixture mapping we identified genomic regions associated with divergence in male nuptial color
and also body shape, suggesting that either tight linkage or pleiotropy has facilitated speciation
in benthic–limnetic species pairs.

We are also mapping fitness through sexual selection arising from both male competition and
female choice. Here we use a naturalized setting to measure sexual selection on multiple
behavioral and morphological phenotypes – an experiment that takes an enormous effort, but
is a lot of fun! Using RAD-seq data we then do genetic mapping to find genomic regions that
underpin multiple phenotypic traits, and multiple fitness components.

Reverse speciation

We have
a rare opportunity to gain insight into the speciation process by watching it
go in the reverse direction. Ecological speciation is a powerful mechanism of
diversification. But species that diverge because of differences in ecology are
vulnerable to ecological change. We are witnessing a natural experiment -
ecological disturbance has triggered the breakdown of a species pair through
hybridization. To try to find the silver lining in a sad event (the
limnetic-benthic species pairs are listed as endangered in Canada), my lab is using
this reverse speciation to understand the forward process of diversification.
We're investigating the loss of both premating and postmating isolation –
characterizing what HAS been lost and identifying the causes. This work has
important implications both for basic science (speciation processes) and
conservation (the effects of invasive species on diversity). To this end, we
hope to facilitate recovery of this pair, and to help avoid similar problems
for the other pairs.

The silver
lining may be even brighter, as hybridization can have both destructive and creative effects on diversification.
A new research direction explores this tension between the homogenizing effect of hybridization and its potential
to generate novel phenotypes and genotypes that could serve as the foundation for subsequent adaptation and
diversification. Intriguing but controversial, the potential for hybridization to foster diversity is seen in
some systems (Heliconius butterflies for one) but whether this is an anomaly or more widespread is very uncertain.
The hybridizing Enos fish may give us a window on this process.

Sexual signal evolution

My lab is collaborating with Tom Getty and
Chris Klausmeier at the
Kellogg Biological Station on a set of projects investigating the dynamics of rapid evolutionary change in
sexual signals - traits like frog calls and bird plumage that are typically used by males to attract and secure mates.
Our work highlights the loss of mating signals rather than their elaboration, and we use both empirical studies in
stickleback fish and field crickets, and mathematical modeling to understand the evolutionary loss of these
important traits. To date, most research on sexual selection has emphasized the exaggeration of male signals
and very strong female preferences for those signals. Both of these should reduce diversity in sexual signaling
systems resulting in one biggest, best male signal. Yet, mating signals are extremely diverse and recent studies
in organisms ranging from insects to vertebrates suggest that male sexual traits are frequently lost, despite the
contention that female preferences should maintain them. We hypothesize that the dynamics of both trait loss and
elaboration contribute to the diversity of sexual systems we see in nature. But, why and how are male signals lost?

Cognitive and sensory evolution

The lab has investigated many aspects of learning, cognition, and sensory evolution in sticklebacks.
This is a great way for me to stay connected to my prior work with bats on social and vocal learning and
cooperative social behavior, and to do so in the experimentally tractable and smart (for fish) sticklebacks.
We’ve had many projects along these lines. Some highlights include the role of social experience in shaping mate
preferences and enhancing sexual isolation. Imprinting has particular importance in this regard – without it
sexual isolation is weak at best. An exciting result from the imprinting work was to identify the developmental
stage (very early) and sensory cues that form the basis of imprinting – this reveals a key role for odor.
Combining olfactory and visual communication in a multimodal manner may prove to be essential to speciation.
The sources of variation in both visual and olfactory cues, and the causes of species differences are an
active area of our current research.

Social learning is another focus of our work. We are particularly interested in comparing social learning between
stickleback species and relating this to differences in ecology and evolution in social behavior. We are also investigating
the changes in stickleback brains that accompany alterations in sensory modality and cognitive ability.
Lastly, we are connecting our work on mate choice, cognition, and genomics by exploring gene expression in the brain
under different social conditions.

Evolutionary robotics

We are collaborating with
an electrical engineer (Xiaobo
Tan) and computer scientist (Phil
McKinley) at MSU to advance our understanding of both behavioral evolution
and robotics. We plan to do this by creating realistic two-way interactions
between live and robotic fish, designed within an evolutionary computational framework.
We focus on predator inspection, an adaptive antipredator behavior, to study
sophisticated non-cooperative and cooperative behaviors in fish, and to synthesize
control and learning strategies for autonomous robotic systems operating in
noisy and unstructured environments. This work is a real meeting-of-the-minds,
and requires concerted, interrelated research effort in biology, robotics, and
computing. Evolutionary computing will enable the design of realistic robotic
fish, and the exploration of important evolutionary questions. The insight from
biology will be exploited to enable adaptive behavior for autonomous robotic
systems, and the use of robots will give us unprecedented flexibility to test
behavioral hypotheses.